skip to main content

Title: Leapfrog dynamics in phage‐bacteria coevolution revealed by joint analysis of cross‐infection phenotypes and whole genome sequencing

Viruses and their hosts can undergo coevolutionary arms races where hosts evolve increased resistance and viruses evolve counter‐resistance. Given these arms race dynamics (ARD), both players are predicted to evolve along a single trajectory as more recently evolved genotypes replace their predecessors. By coupling phenotypic and genomic analyses of coevolving populations of bacteriophageλandEscherichia coli, we find conflicting evidence for ARD. Virus‐host infection phenotypes fit the ARD model, yet genomic analyses revealed fluctuating selection dynamics. Rather than coevolution unfolding along a single trajectory, cryptic genetic variation emerges and is maintained at low frequency for generations until it eventually supplants dominant lineages. These observations suggest a hybrid ‘leapfrog’ dynamic, revealing weaknesses in the predictive power of standard coevolutionary models. The findings shed light on the mechanisms that structure coevolving ecological networks and reveal the limits of using phenotypic or genomic data alone to differentiate coevolutionary dynamics.

more » « less
Award ID(s):
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;
Publisher / Repository:
Date Published:
Journal Name:
Ecology Letters
Page Range / eLocation ID:
p. 876-888
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The rate and trajectory of evolution in an obligate parasite is critically dependent on those of its host(s). Adaptation to a genetically homogeneous host population should theoretically result in specialization, while adaptation to an evolving host population (i.e., coevolution) can result in various outcomes including diversification, range expansion, and/or local adaptation. For viruses of bacteria (bacteriophages, or phages), our understanding of how evolutionary history of the bacterial host(s) impacts viral genotypic and phenotypic evolution is currently limited. In this study, we used whole genome sequencing and two different metrics of phage impacts to compare the genotypes and phenotypes of lytic phages that had either coevolved with or were repeatedly passaged on an unchanging (ancestral) strain of the phytopathogenPseudomonas syringae. Genomes of coevolved phages had more mutations than those of phages passaged on a constant host, and most mutations were in genes encoding phage tail‐associated proteins. Phages from both passaging treatments shared some phenotypic outcomes, including range expansion and divergence across replicate populations, but coevolved phages were more efficient at reducing population growth (particularly of sympatric coevolved hosts). Genotypic similarity correlated with infectivity profile similarity in coevolved phages, but not in phages passaged on the ancestral host. Overall, while adaptation to either host type (coevolving or ancestral) led to divergence in phage tail proteins and infectivity patterns, coevolution led to more rapid molecular changes that increased bacterial killing efficiency and had more predictable effects on infectivity range. Together, these results underscore the important role of hosts in driving viral evolution and in shaping the genotype–phenotype relationship.

    more » « less
  2. Abstract

    Landscape patterns of phenotypic coevolution are determined by variation in the outcome of predator–prey interactions. These outcomes may depend not only on the functional phenotypes that mediate species interactions, but also on aspects of the environment that enable encounters between coevolutionary partners.

    Exploring the relationship between coevolutionary traits and the environment requires extensive sampling across the range of the interaction to determine the relationship between local ecological variation and coevolution.

    In this study, we synthesized >30 years of data on predator–prey interactions between toxic newts (Taricha granulosa) and their snake predators (Thamnophis sirtalis) to explore the environmental predictors of arms race escalation.

    We found that geographic variation in phenotypes at the interface of coevolution was best predicted by a combination of community and climatic variation. Coevolutionary phenotypes were greatest in environments with climate favourable for newt–snake overlap. We found prey toxicity was elevated in regions with more predator species, and predator resistance was higher in regions with more prey species.

    Our results suggest specific environmental conditions reinforce the process of coevolution, signifying the phenotypic outcomes of coevolutionary arms races are sensitive to local ecological contexts that vary across the landscape.

    Read the freePlain Language Summaryfor this article on the Journal blog.

    more » « less
  3. Abstract

    Antagonistic coevolution between natural enemies can produce highly exaggerated traits, such as prey toxins and predator resistance. This reciprocal process of adaptation and counter‐adaptation may also open doors to other evolutionary novelties not directly involved in the phenotypic interface of coevolution. We tested the hypothesis that predator–prey coevolution coincided with the evolution of conspicuous coloration on resistant predators that retain prey toxins. In western North America, common garter snakes (Thamnophis sirtalis) have evolved extreme resistance to tetrodotoxin (TTX) in the coevolutionary arms race with their deadly prey, Pacific newts (Tarichaspp.). TTX‐resistant snakes can retain large amounts of ingested TTX, which could serve as a deterrent against the snakes' own predators if TTX toxicity and resistance are coupled with a conspicuous warning signal. We evaluated whether arms race escalation covaries with bright red coloration in snake populations across the geographic mosaic of coevolution. Snake colour variation departs from the neutral expectations of population genetic structure and covaries with escalating clines of newt TTX and snake resistance at two coevolutionary hotspots. In the Pacific Northwest, bright red coloration fits an expected pattern of an aposematic warning to avian predators: TTX‐resistant snakes that consume highly toxic newts also have relatively large, reddish‐orange dorsal blotches. Snake coloration also seems to have evolved with the arms race in California, but overall patterns are less intuitively consistent with aposematism. These results suggest that interactions with additional trophic levels can generate novel traits as a cascading consequence of arms race coevolution across the geographic mosaic.

    more » « less
  4. Abstract

    Understanding how interspecific interactions mould the molecular basis of adaptations in coevolving species is a long‐sought goal of evolutionary biology. Venom in predators and venom resistance proteins in prey are coevolving molecular phenotypes, and while venoms are highly complex mixtures it is unclear if prey respond with equally complex resistance traits. Here, we use a novel molecular methodology based on protein affinity columns to capture and identify candidate blood serum resistance proteins (“venom interactive proteins” [VIPs]) in California Ground Squirrels (Otospermophilus beecheyi) that interact with venom proteins from their main predator, Northern Pacific Rattlesnakes (Crotalus o. oreganus). This assay showed that serum‐based resistance is both population‐ and species‐specific, with serum proteins from ground squirrels showing higher binding affinities for venom proteins of local snakes compared to allopatric individuals. Venom protein specificity assays identified numerous and diverse candidate prey resistance VIPs but also potential targets of venom in prey tissues. Many specific VIPs bind to multiple snake venom proteins and, conversely, single venom proteins bind multiple VIPs, demonstrating that a portion of the squirrel blood serum “resistome” involves broad‐based inhibition of nonself proteins and suggests that resistance involves a toxin scavenging mechanism. Analyses of rates of evolution of VIP protein homologues in related mammals show that most of these proteins evolve under purifying selection possibly due to molecular constraints that limit the evolutionary responses of prey to rapidly evolving snake venom proteins. Our method represents a general approach to identify specific proteins involved in co‐evolutionary interactions between species at the molecular level.

    more » « less
  5. Abstract

    The Geographic Mosaic Theory of Coevolution predicts that coevolutionary arms races will vary over time and space because of the diverse ecological settings and population histories of interacting species across the landscape. Thus, understanding coevolution may require investigating broad sets of populations sampled across the range of the interaction. In addition, comparing coevolutionary dynamics between similar systems may reveal the importance of specific factors that structure coevolution.

    Here, we examine geographic patterns of prey traits and predator traits in the relatively unstudied interaction between the Sierra garter snake (Thamnophis couchii) and sympatric prey, the rough‐skinned newt (Taricha granulosa), Sierra newt (Ta. sierrae) and California newt (Ta. torosa). This system parallels, in space and phenotypes, a classic example of coevolution between predatory common garter snakes (Th. sirtalis) and their toxic newt prey exhibiting hotspots of newt tetrodotoxin (TTX) levels and matching snake TTX resistance.

    We quantified prey and predator traits from hundreds of individuals across their distributions, and functional trait matching at sympatric sites.

    We show strong regional patterns of trait covariation across the shared ranges ofTh. couchiiand newt prey. Traits differ significantly among localities, with lower newt TTX levels and snake TTX resistance at the northern latitudes, and higher TTX levels and snake resistance at southern latitudes. Newts and snakes in northern populations show the highest degree of functional trait matching despite possessing the least extreme traits. Conversely, newts and snakes in southern populations show the greatest mismatch despite possessing exaggerated traits, with some snakes so resistant to TTX they would be unaffected by any sympatric newt. Nevertheless, individual variation was substantial, and appears to offer the opportunity for continued reciprocal selection in most populations.

    Overall, the three species of newts appear to be engaged in a TTX‐mediated arms race withTh. couchii. These patterns are congruent with those seen between newts andTh. sirtalis, including the same latitudinal gradient in trait covariation, and the potential ‘escape’ from the arms race by snake predators. Such concordance in broad scale patterns across two distinct systems suggests common phenomena might structure geographic mosaics in similar ways.

    more » « less